Nanoribbon Biosensor in the Detection of miRNAs Associated with Colorectal Cancer
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemicals
2.2. Oligonucleotides
2.3. Nanoribbon Biosensor
2.4. Chip Surface Modification
2.5. Covalent Immobilization of Oligonucleotide Probes
2.6. Preparation of Solutions of Target sDNAs in Buffer
2.7. Electrical Measurements
2.8. Measurements with the Nanoribbon Biosensor
2.9. Plasma Samples
3. Results
3.1. Functionalization of the Nanochip Surface
3.2. Determination of the Detection Limit Attainable with the NRBS in Buffer Solutions upon the Detection of Target sDNA
3.3. Detection of miRNA Isolated from Blood Plasma using NRBS
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Shaukat, A.; Kahi, C.J.; Burke, C.A.; Rabeneck, L.; Sauer, B.G.; Rex, D.K. ACG Clinical Guidelines: Colorectal Cancer Screening 2021. Off. J. Am. Coll. Gastroenterol.|ACG 2021, 116, 458–479. [Google Scholar] [CrossRef] [PubMed]
- Meklin, J.; Syrjänen, K.; Eskelinen, M. Fecal Occult Blood Tests in Colorectal Cancer Screening: Systematic Review and Meta-Analysis of Traditional and New-Generation Fecal Immunochemical Tests. Anticancer Res 2020, 40, 3591–3604. [Google Scholar] [CrossRef]
- Gao, Y.; Wang, J.; Zhou, Y.; Sheng, S.; Qian, S.Y.; Huo, X. Evaluation of Serum CEA, CA19-9, CA72-4, CA125 and Ferritin as Diagnostic Markers and Factors of Clinical Parameters for Colorectal Cancer. Sci Rep. 2018, 8, 2732. [Google Scholar] [CrossRef]
- Björkman, K.; Mustonen, H.; Kaprio, T.; Kekki, H.; Pettersson, K.; Haglund, C.; Böckelman, C. CA125: A Superior Prognostic Biomarker for Colorectal Cancer Compared to CEA, CA19-9 or CA242. Tumor Biol. 2021, 43, 57–70. [Google Scholar] [CrossRef] [PubMed]
- Weng, W.; Feng, J.; Qin, H.; Ma, Y.; Goel, A. An Update on MiRNAs as Biological and Clinical Determinants in Colorectal Cancer: A Bench-to-Bedside Approach. Future Oncol. 2015, 11, 1791–1808. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hur, K.; Toiyama, Y.; Schetter, A.J.; Okugawa, Y.; Harris, C.C.; Boland, C.R.; Goel, A. Identification of a Metastasis-Specific MicroRNA Signature in Human Colorectal Cancer. JNCI: J. Natl. Cancer Inst. 2015, 107, dju492. [Google Scholar] [CrossRef] [PubMed]
- Han, T.-S.; Hur, K.; Xu, G.; Choi, B.; Okugawa, Y.; Toiyama, Y.; Oshima, H.; Oshima, M.; Lee, H.-J.; Kim, V.N.; et al. MicroRNA-29c Mediates Initiation of Gastric Carcinogenesis by Directly Targeting ITGB1. Gut 2015, 64, 203–214. [Google Scholar] [CrossRef] [Green Version]
- Lu, D.; Tang, L.; Zhuang, Y.; Zhao, P. MiR-17-3P Regulates the Proliferation and Survival of Colon Cancer Cells by Targeting Par4. Mol. Med. Rep. 2017, 17, 618–623. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Selth, L.A.; Townley, S.; Gillis, J.L.; Ochnik, A.M.; Murti, K.; Macfarlane, R.J.; Chi, K.N.; Marshall, V.R.; Tilley WDButler, L.M. Discovery of Circulating MicroRNAs Associated with Human Prostate Cancer Using a Mouse Model of Disease. Int. J. Cancer 2012, 131, 652–661. [Google Scholar] [CrossRef]
- Rissin, D.M.; Kan, C.W.; Campbell, T.G.; Howes, S.C.; Fournier, D.R.; Song, L.; Piech, T.; Patel, P.P.; Chang, L.; Rivnak, A.J.; et al. Single-Molecule Enzyme-Linked Immunosorbent Assay Detects Serum Proteins at Subfemtomolar Concentrations. Nat. Biotechnol. 2010, 28, 595–599. [Google Scholar] [CrossRef] [Green Version]
- Mannelli, C. Tissue vs Liquid Biopsies for Cancer Detection: Ethical Issues. J. Bioethical Inq. 2019, 16, 551–557. [Google Scholar] [CrossRef]
- Ye, J.; Xu, M.; Tian, X.; Cai, S.; Zeng, S. Research Advances in the Detection of MiRNA. J. Pharm. Anal. 2019, 9, 217–226. [Google Scholar] [CrossRef] [PubMed]
- Penso-Dolfin, L.; Moxon, S.; Haerty, W.; Di Palma, F. The Evolutionary Dynamics of MicroRNAs in Domestic Mammals. Sci. Rep. 2018, 8, 17050. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gu, L.-Q.; Wanunu, M.; Wang, M.X.; McReynolds, L.; Wang, Y. Detection of MiRNAs with a Nanopore Single-Molecule Counter. Expert Rev. Mol. Diagn. 2012, 12, 573–584. [Google Scholar] [CrossRef] [PubMed]
- Peng, J.; Hou, F.; Feng, J.; Xu, S.; Meng, X. Long Non-Coding RNA BCYRN1 Promotes the Proliferation and Metastasis of Cervical Cancer via Targeting MicroRNA-138 In vitro and In vivo. Oncol. Lett. 2018, 15, 5809–5818. [Google Scholar] [CrossRef] [PubMed]
- Ahmad, W.; Gull, B.; Baby, J.; Mustafa, F. A Comprehensive Analysis of Northern versus Liquid Hybridization Assays for MRNAs, Small RNAs, and MiRNAs Using a Non-Radiolabeled Approach. Curr. Issues Mol. Biol. 2021, 43, 457–484. [Google Scholar] [CrossRef]
- Wu, Q.; Lu, Z.; Li, H.; Lu, J.; Guo, L.; Ge, Q. Next-Generation Sequencing of MicroRNAs for Breast Cancer Detection. J. Biomed. Biotechnol. 2011, 2011, 597145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ouyang, T.; Liu, Z.; Han, Z.; Ge, Q. MicroRNA Detection Specificity: Recent Advances and Future Perspective. Anal. Chem. 2019, 91, 3179–3186. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kalofonou, M.; Malpartida-Cardenas, K.; Alexandrou, G.; Rodriguez-Manzano, J.; Yu, L.-S.; Miscourides, N.; Allsopp, R.; Gleason, K.L.T.; Goddard, K.; Fernandez-Garcia, D.; et al. A Novel Hotspot Specific Isothermal Amplification Method for Detection of the Common PIK3CA p.H1047R Breast Cancer Mutation. Sci. Rep. 2020, 10, 4553. [Google Scholar] [CrossRef] [Green Version]
- Deng, R.; Zhang, K.; Li, J. Isothermal Amplification for MicroRNA Detection: From the Test Tube to the Cell. Acc. Chem. Res. 2017, 50, 1059–1068. [Google Scholar] [CrossRef]
- Nilsen, A.; Jonsson, M.; Aarnes, E.-K.; Kristensen, G.B.; Lyng, H. Reference MicroRNAs for RT-QPCR Assays in Cervical Cancer Patients and Their Application to Studies of HPV16 and Hypoxia Biomarkers. Transl. Oncol. 2019, 12, 576–584. [Google Scholar] [CrossRef] [PubMed]
- Krepelkova, I.; Mrackova, T.; Izakova, J.; Dvorakova, B.; Chalupova, L.; Mikulik, R.; Slaby, O.; Bartos, M.; Ruzicka, V. Evaluation of MiRNA Detection Methods for the Analytical Characteristic Necessary for Clinical Utilization. BioTechniques 2019, 66, 277–284. [Google Scholar] [CrossRef] [Green Version]
- Zheng, G.; Patolsky, F.; Cui, Y.; Wang, W.U.; Lieber, C.M. Multiplexed Electrical Detection of Cancer Markers with Nanowire Sensor Arrays. Nat. Biotechnol. 2005, 23, 1294–1301. [Google Scholar] [CrossRef] [PubMed]
- Patolsky, F.; Zheng, G.; Hayden, O.; Lakadamyali, M.; Zhuang, X.; Lieber, C.M. Electrical Detection of Single Viruses. Proc. Natl. Acad. Sci. USA 2004, 101, 14017–14022. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tintelott, M.; Pachauri, V.; Ingebrandt, S.; Vu, X.T. Process Variability in Top-Down Fabrication of Silicon Nanowire-Based Biosensor Arrays. Sensors 2021, 21, 5153. [Google Scholar] [CrossRef] [PubMed]
- Faltejskova, P.; Bocanek, O.; Sachlova, M.; Svoboda, M.; Kiss, I.; Vyzula, R.; Slaby, O. Circulating MiR-17-3p, MiR-29a, MiR-92a and MiR-135b in Serum: Evidence against Their Usage as Biomarkers in Colorectal Cancer. Cancer Biomark. 2013, 12, 199–204. [Google Scholar] [CrossRef] [PubMed]
- Fletcher, C.E.; Sulpice, E.; Combe, S.; Shibakawa, A.; Leach, D.A.; Hamilton, M.P.; Chrysostomou, S.L.; Sharp, A.; Welti, J.; Yuan, W.; et al. Androgen Receptor-Modulatory MicroRNAs Provide Insight into Therapy Resistance and Therapeutic Targets in Advanced Prostate Cancer. Oncogene 2019, 38, 5700–5724. [Google Scholar] [CrossRef] [Green Version]
- Bruel, M.; Aspar, B.; Auberton-Hervé, A.-J. Smart-Cut: A New Silicon On Insulator Material Technology Based on Hydrogen Implantation and Wafer Bonding. Jpn. J. Appl. Phys. 1997, 36 Pt 1, 1636–1641. [Google Scholar] [CrossRef]
- Popov, V.P.; Antonova, A.I.; Frantsuzov, A.A.; Safronov, L.N.; Feofanov, G.N.; Naumova, O.V.; Kilanov, D.V. Properties of Silicon-on-Insulator Structures and Devices. Semiconductors 2001, 35, 1030–1037. [Google Scholar] [CrossRef]
- Ivanov, Y.D.; Pleshakova, T.O.; Kozlov, A.F.; Malsagova, K.A.; Krohin, N.V.; Shumyantseva, V.V.; Shumov, I.D.; Popov, V.P.; Naumova, O.V.; Fomin, B.I.; et al. SOI Nanowire for the High-Sensitive Detection of HBsAg and α-Fetoprotein. Lab Chip 2012, 12, 5104–5111. [Google Scholar] [CrossRef]
- Naumova, O.V.; Fomin, B.I.; Nasimov, D.A.; Dudchenko, N.V.; Devyatova, S.F.; Zhanaev, E.D.; Popov, V.P.; Latyshev, A.V.; Aseev, A.L.; Ivanov, Y.D.; et al. SOI Nanowires as Sensors for Charge Detection. Semicond. Sci. Technol. 2010, 25, 055004. [Google Scholar] [CrossRef]
- Ivanov, Yu. D.; Danichev, V.V.; Pleshakova, T.O.; Shumov, I.D.; Ziborov, V.S.; Krokhin, N.V.; Zagumenniy, M.N.; Ustinov, V.S.; Smirnov, L.P.; Shironin, A.V. Irreversible Chemical AFM-Based Fishing for Detection of Low-Copied Proteins. Biochem. (Mosc. ) Suppl. Ser. B: Biomed. Chem. 2013, 7, 46–61. [Google Scholar] [CrossRef]
- Ivanov, Y.D.; Malsagova, K.A.; Popov, V.P.; Pleshakova, T.O.; Kozlov, A.F.; Galiullin, R.A.; Shumov, I.D.; Kapustina, S.I.; Tikhonenko, F.V.; Ziborov, V.S.; et al. Nanoribbon-Based Electronic Detection of a Glioma-Associated Circular MiRNA. Biosensors 2021, 11, 237. [Google Scholar] [CrossRef]
- Laborde, C.; Pittino, F.; Verhoeven, H.A.; Lemay, S.G.; Selmi, L.; Jongsma, M.A.; Widdershoven, F.P. Real-Time Imaging of Microparticles and Living Cells with CMOS Nanocapacitor Arrays. Nat. Nanotechnol. 2015, 10, 791–795. [Google Scholar] [CrossRef] [Green Version]
- Malsagova, K.A.; Pleshakova, T.O.; Galiullin, R.A.; Kozlov, A.F.; Romanova, T.S.; Shumov, I.D.; Popov, V.P.; Tikhonenko, F.V.; Glukhov, A.V.; Smirnov, A. Yu.; et al. SOI-Nanowire Biosensor for the Detection of Glioma-Associated MiRNAs in Plasma. Chemosensors 2020, 8, 95. [Google Scholar] [CrossRef]
- Wang, T.; Zhang, K.-H. New Blood Biomarkers for the Diagnosis of AFP-Negative Hepatocellular Carcinoma. Front. Oncol. 2020, 10, 1316. [Google Scholar] [CrossRef] [PubMed]
- Malsagova, K.A.; Pleshakova, T.O.; Galiullin, R.A.; Shumov, I.D.; Kozlov, A.F.; Romanova, T.S.; Popov, V.P.; Glukhov, A.V.; Konev, V.A.; Archakov, A.I.; et al. Nanowire Aptamer-Sensitized Biosensor Chips with Gas Plasma-Treated Surface for the Detection of Hepatitis C Virus Core Antigen. Coatings 2020, 10, 753. [Google Scholar] [CrossRef]
- Knopfmacher, O.; Tarasov, A.; Fu, W.; Wipf, M.; Niesen, B.; Calame, M.; Schönenberger, C. Nernst Limit in Dual-Gated Si-Nanowire FET Sensors. Nano Lett. 2010, 10, 2268–2274. [Google Scholar] [CrossRef] [PubMed]
- Ambhorkar, P.; Wang, Z.; Ko, H.; Lee, S.; Koo, K.; Kim, K.; Cho, D. Nanowire-Based Biosensors: From Growth to Applications. Micromachines 2018, 9, 679. [Google Scholar] [CrossRef] [Green Version]
- Wu, C.-C.; Manga, Y.B.; Yang, M.-H.; Chien, Z.-S.; Lee, K.-S. Label-Free Detection of BRAF V599E Gene Mutation Using Side-Gated Nanowire Field Effect Transistors. J. Electrochem. Soc. 2018, 165, B576–B581. [Google Scholar] [CrossRef]
- Precazzini, F.; Detassis, S.; Imperatori, A.S.; Denti, M.A.; Campomenosi, P. Measurements Methods for the Development of MicroRNA-Based Tests for Cancer Diagnosis. Int. J. Mol. Sci. 2021, 22, 1176. [Google Scholar] [CrossRef]
- Dave, V.P.; Ngo, T.A.; Pernestig, A.-K.; Tilevik, D.; Kant, K.; Nguyen, T.; Wolff, A.; Bang, D.D. MicroRNA Amplification and Detection Technologies: Opportunities and Challenges for Point of Care Diagnostics. Lab. Investig. 2019, 99, 452–469. [Google Scholar] [CrossRef] [PubMed]
- Bally, M.; Graule, M.; Parra, F.; Larson, G.; Höök, F. A Virus Biosensor with Single Virus-Particle Sensitivity Based on Fluorescent Vesicle Labels and Equilibrium Fluctuation Analysis. Biointerphases 2013, 8, 4. [Google Scholar] [CrossRef] [Green Version]
- Zverzhinetsky, M.; Krivitsky, V.; Patolsky, F. Direct Whole Blood Analysis by the Antigen-Antibody Chemically-Delayed Dissociation from Nanosensors Arrays. Biosens. Bioelectron. 2020, 170, 112658. [Google Scholar] [CrossRef] [PubMed]
- Pleshakova, T.O.; Shumov, I.D.; Ivanov, Y.D.; Malsagova, K.A.; Kaysheva, A.L.; Archakov, A.I. AFM-based technologies as the way towards the reverse Avogadro number. Biochem. (Mosc. ) Suppl. Ser. B: Biomed. Chem. 2015, 9, 244–257. [Google Scholar] [CrossRef]
- Ferreira, J.; Santos, M.J.L.; Rahman, M.M.; Brolo, A.G.; Gordon, R.; Sinton, D.; Girotto, E.M. Attomolar Protein Detection Using In-Hole Surface Plasmon Resonance. J. Am. Chem. Soc. 2009, 131, 436–437. [Google Scholar] [CrossRef] [PubMed]
- Guo, L.; Kim, D.-H. LSPR Biomolecular Assay with High Sensitivity Induced by Aptamer–Antigen–Antibody Sandwich Complex. Biosens. Bioelectron. 2012, 31, 567–570. [Google Scholar] [CrossRef]
- Djoba Siawaya, J.F.; Roberts, T.; Babb, C.; Black, G.; Golakai, H.J.; Stanley, K.; Bapela, N.B.; Hoal, E.; Parida, S.; van Helden, P.; et al. An Evaluation of Commercial Fluorescent Bead-Based Luminex Cytokine Assays. PLoS ONE 2008, 3, e2535. [Google Scholar] [CrossRef] [Green Version]
- Archakov, A.I.; Ivanov, Y.D.; Lisitsa, A.V.; Zgoda, V.G. AFM Fishing Nanotechnology Is the Way to Reverse the Avogadro Number in Proteomics. Proteomics 2007, 7, 4–9. [Google Scholar] [CrossRef]
- Cheng, S.; Hideshima, S.; Kuroiwa, S.; Nakanishi, T.; Osaka, T. Label-Free Detection of Tumor Markers Using Field Effect Transistor (FET)-Based Biosensors for Lung Cancer Diagnosis. Sens. Actuators B: Chem. 2015, 212, 329–334. [Google Scholar] [CrossRef]
- Gao, A.; Yang, X.; Tong, J.; Zhou, L.; Wang, Y.; Zhao, J.; Mao, H.; Li, T. Multiplexed Detection of Lung Cancer Biomarkers in Patients Serum with CMOS-Compatible Silicon Nanowire Arrays. Biosens. Bioelectron. 2017, 91, 482–488. [Google Scholar] [CrossRef] [PubMed]
- Lu, N.; Gao, A.; Dai, P.; Mao, H.; Zuo, X.; Fan, C.; Wang, Y.; Li, T. Ultrasensitive Detection of Dual Cancer Biomarkers with Integrated CMOS-Compatible Nanowire Arrays. Anal. Chem. 2015, 87, 11203–11208. [Google Scholar] [CrossRef] [PubMed]
- Zhu, K.; Zhang, Y.; Li, Z.; Zhou, F.; Feng, K.; Dou, H.; Wang, T. Simultaneous Detection of α-Fetoprotein and Carcinoembryonic Antigen Based on Si Nanowire Field-Effect Transistors. Sensors 2015, 15, 19225–19236. [Google Scholar] [CrossRef] [Green Version]
- Silverman, S.K. Deoxyribozymes: Selection Design and Serendipity in the Development of DNA Catalysts. Acc. Chem. Res. 2009, 42, 1521–1531. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dorvel, B.R.; Reddy, B.; Go, J.; Duarte Guevara, C.; Salm, E.; Alam, M.A.; Bashir, R. Silicon Nanowires with High-k Hafnium Oxide Dielectrics for Sensitive Detection of Small Nucleic Acid Oligomers. ACS Nano 2012, 6, 6150–6164. [Google Scholar] [CrossRef] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ivanov, Y.D.; Goldaeva, K.V.; Malsagova, K.A.; Pleshakova, T.O.; Galiullin, R.A.; Popov, V.P.; Kushlinskii, N.E.; Alferov, A.A.; Enikeev, D.V.; Potoldykova, N.V.; et al. Nanoribbon Biosensor in the Detection of miRNAs Associated with Colorectal Cancer. Micromachines 2021, 12, 1581. https://doi.org/10.3390/mi12121581
Ivanov YD, Goldaeva KV, Malsagova KA, Pleshakova TO, Galiullin RA, Popov VP, Kushlinskii NE, Alferov AA, Enikeev DV, Potoldykova NV, et al. Nanoribbon Biosensor in the Detection of miRNAs Associated with Colorectal Cancer. Micromachines. 2021; 12(12):1581. https://doi.org/10.3390/mi12121581
Chicago/Turabian StyleIvanov, Yuri D., Kristina V. Goldaeva, Kristina A. Malsagova, Tatyana O. Pleshakova, Rafael A. Galiullin, Vladimir P. Popov, Nikolay E. Kushlinskii, Alexander A. Alferov, Dmitry V. Enikeev, Natalia V. Potoldykova, and et al. 2021. "Nanoribbon Biosensor in the Detection of miRNAs Associated with Colorectal Cancer" Micromachines 12, no. 12: 1581. https://doi.org/10.3390/mi12121581